SUMMARY

Foraging blue crabs must respond to fluid forces imposed on their body
while acquiring useful chemical signals from turbulent odor plumes. This study
examines how blue crabs manage these simultaneous demands. The drag force, and
hence the cost of locomotion, experienced by blue crabs is shown to be a
function of the body orientation angle relative to the flow. Rather than
adopting a fixed orientation that minimizes the drag, blue crabs decrease
their relative angle (increase drag) when odor is present in low speed flow,
while assuming a drag-minimizing posture under other conditions. The
motivation for crabs to adopt an orientation with larger drag appears to
relate to their ability to acquire chemical signal information for odor
tracking. In particular, when orienting at a smaller angle relative to the
flow direction, more concentrated odor filaments arrive at the antennules to
mediate upstream movement, allowing a more useful bilateral comparison between
the appendage chemosensors to be made. Blue crabs respond to conflicting
demands by weighting the degree of drag minimization in proportion to the
potential magnitude of the drag cost and the potential benefit of acquiring
chemosensory cues. Higher flow velocity magnifies the locomotory cost of a
high drag posture, thus in swift flows crabs minimize drag and sacrifice their
ability to acquire olfactory cues.

Introduction

Aquatic and terrestrial invertebrates, such as arthropods, rely heavily on
chemoperception for many tasks. The ability of these animals to locate prey or
mates, or flee predators, varies due to flow-induced modification of sensory
cues (Weissburg and Zimmer-Faust,
1993; Vickers and Baker,
1994; Mafra-Neto and
Cardé, 1998). Animals exposed to weaker or more
intermittent stimuli show decreased search efficiency and lower overall
response rates to chemical plumes. For instance, blue crabs (Callinectes
sapidus) in more turbulent conditions in both the lab and field take more
circuitous routes to prey and have lower success rates, suggesting that
turbulence intensity is a key flow property that modulates
chemosensory-mediated guidance (Weissburg
and Zimmer-Faust, 1993).

However, the fluid medium transmits forces in addition to sensory signals,
and information gathering is not the only activity that can be strongly
affected by fluid flow. Hydrodynamic forces may be particularly important in
water due to its relatively high density. Consequently, animals moving through
aquatic habitats or exposed to strong ambient flows may experience significant
forces that hamper stability and impose a cost on locomotion or appendage
movement. Adaptive responses that ameliorate the negative consequences of
these forces include postural adjustments, changes in gait or modifications of
propulsive movements (Vogel,
1994; Fuiman and Batty,
1997; Martinez et al.,
1998).

The present study examines the potentially competing influences of
hydrodynamic forces and odor transport to explain blue crab behavioral
responses to the simultaneous demands of efficient locomotion and acquisition
of sensory cues. Our data suggest that flow creates conflicting constraints
between the ability to move efficiently and to acquire chemosensory
information necessary for navigation, such that they cannot be simultaneously
maximized. Furthermore, the strategy employed by foraging animals is flexible
and contingent upon the relative penalty imposed by the flow, which suggests
that animals assess the tradeoffs involved in adopting a particular tactic in
a given flow environment.

Materials and methods

Flow environments

Experiments were conducted in the Environmental Fluid Mechanics Laboratory
at Georgia Institute of Technology. A 0.38 m-wide freshwater flume was used
for the drag measurements because the flow rate in this facility could be
easily varied and rapidly measured. Flow visualization and quantification of
the odor plume structure using planar laser-induced fluorescence and the
electrochemical probe took place in a large freshwater tilting flume (24 m
long×1.07 m wide) capable of generating an equilibrium bed boundary
layer. The flow speed, U, was 0.05 m s-1 and the flow
depth, H, was 0.20 m for these measurements. The tilting flume cannot
be used with seawater, so behavioral experiments were performed in a separate
saltwater facility (10 m long×0.75 m wide) capable of generating the
same flow characteristics as the freshwater flume. In addition to matching the
flow conditions above, the behavioral experiments were also performed for a
flow speed of 0.10 m s-1. In each case, the plume was discharged
from a round brass nozzle (4.7 mm diameter) located 0.025 m above the flume
bed at a velocity that matched the flume velocity (i.e. an iso-kinetic
release). The nozzle perturbed the flow negligibly due to a smooth brass
faring on the downstream side, which prevented flow separation.

Drag measurements

The drag force on the crab was measured by summing the moments around a
pivot point (Fig. 1). As shown
in Fig. 1, the crab was
supported at a distance of l1 below the pivot point. The
spring at the end of the lever arm was adjusted to establish a horizontal
reference position with no flow. A weight (W, 5.89 N) on the
horizontal lever arm provided a moment in the opposite sense to that of the
drag force. Measuring the location of the weight relative to the pivot
(l2) and equating the sum of moments to zero yielded the
drag force (FD):
1
The drag force on the submerged section of the support shaft,
Fshaft, operates at a distance lshaft
from the pivot point and is calculated from standard drag coefficient tables
for round cylinders (e.g. Munson et al.,
2002). The crab specimen was located just above the floor of the
flume to mimic walking or swimming blue crabs in a benthic boundary layer.
Orientation angles (α) are defined relative to the flow; 0°
corresponds to the crab facing directly upstream, whereas 90° corresponds
to the crab facing directly to the side (see inset of
Fig. 2). Drag forces were
measured at angles from 0° through 90° in 15° increments for eight
flow velocities between 0.328 m s-1 and 0.591 m s-1 each
with a flow depth of 0.20 m. These velocities are at the high end of the
relative water speeds that blue crabs encounter in tidal channels (i.e.
walking speed of 0.1 m s-1 in water velocity of 0.03 m
s-1; Zimmer-Faust et al.,
1995). The drag coefficient was found to be constant with Reynolds
number (Re) in this range, thus the results can be reliably extended
to slightly smaller or larger flow rates.

Schematic of the force balance for the drag measurements. The crab was
supported at a distance l1 below the pivot point. A weight
(W) on the horizontal lever arm, at a distance l2
from the pivot point, provided a moment in the opposite sense to that of the
drag force (FD). Fshaft represents the
drag force on the submerged section of the support shaft, which is at a
distance lshaft below the pivot point.

Drag coefficient (CD) for five crab specimens at
orientation angles (α) from 0° to 90°. Based on the expected
symmetry of the flow patterns around the crab (i.e. roughly symmetrical left
to right and front to back), a functional form of cos(2α) is assumed for
the drag variation with orientation angle. A trend line based on linear
regression is shown and yields an r2 value of 0.84. A
third-order polynomial fit with respect to α yielded a similar
r2.

Five dead crabs (three males and two females) were used for the drag
measurements, each with a slightly different size, posture and appendage
configuration (Table 1). The
legs and claws were fixed with epoxy in positions resembling walking or
standing. The frontal projected area of each crab was measured by digitally
photographing the animal against a white background and counting the number of
pixels within the body shape outline.

The drag coefficient (CD) is defined as
(Munson et al., 2002):
2
where ρ is the fluid density and Afront is the frontal
projected area. It is important to choose the correct representative area for
the drag coefficient (e.g. Vogel,
1994). In this case, we employ the frontal projected area because
the streamlines are expected to separate from the crab body, and, hence, the
drag force will be dominated by form drag. This is consistent with the
uniformity of CD with varying Re and was
confirmed by testing two alternative area definitions, both of which failed to
demonstrate dynamic similarity of the CD data.

Flow visualization

Neutrally buoyant dye was used to observe the plume transport around dead
and live crabs. The carapaces of the dead specimens were painted black for
visual contrast and were mounted with silicone glue to a white aluminum disk.
During the trials, the disk was rotated to produce crab orientations of 0°
through 90° at 15° increments. Live crabs were tethered to the disk by
snuggly attaching a zip-tie around the crab carapace near the rear legs.
Monofilament line was looped through the zip-tie and two small holes in the
disk. Thus, the crab was loosely constrained to the disk while allowing normal
vertical movements and breathing.

A Kodak digital camera captured the images of the dye plume flowing past
the crab. Images were collected from above and from the side for each
orientation at two distances from the source: 0.3m and 1m. Two dead specimens
were employed, one with the front claws tucked near to the carapace, and one
with the claws extended in front of the carapace. The live crabs were tested
in both freshwater and saltwater flow. Animals tested in the freshwater flume
were first acclimated to 5‰ seawater (the salinity of the freshwater
flume) over a period of 10 days by reducing the salinity of the holding tanks
by 3-5‰ each day. There was no apparent difference in the plume
structure near crabs in saltwater vs freshwater, so only the latter
is reported. In addition to the still images, the live animals were also
recorded with a Sony digital camcorder.

Planar laser-induced fluorescence (PLIF)

Planar laser-induced fluorescence measurements provided a quantitative
characterization of the odor field around the crab body. The principle of this
technique is that fluorescent dye (Rhodamine 6G in this case) absorbs light in
the green wavelengths and emits light in the yellow/orange wavelengths. The
intensity of the emitted light is proportional to the chemical concentration
and the incident light intensity. Thus, after a calibration, the instantaneous
concentration distribution in the plane of the laser sheet can be
non-intrusively measured.

Webster et al. (in press)
previously described the PLIF system in detail. A scanning mirror swept an
argon-ion laser beam through the flow in a plane parallel to the channel bed
at the elevation of the source nozzle. Images of the emitted light were
collected using a Kodak Megaplus ES 1.0 camera over an area of roughly 1
m×1 m. The image capture rate was 10 Hz synchronized with the laser
sweep. Data were collected with crabs at three orientations: 0°, 45°
and 90°. In each orientation, 6000 consecutive images were collected over
a 10-min period, which is sufficient to produce converged mean and S.D. values
(Webster and Weissburg, 2001).
The in situ calibration was performed as described by Webster et al.
(in press).

Electrochemical measurements of signal structure

A 10μm electrochemical sensor, which is sensitive to submicromolar
concentrations of dopamine, was used to quantify the signal structure arriving
at the chemosensory appendages (Moore et
al., 1994). The goal of this series of experiments was to examine
whether body orientation changes the character of chemical information
arriving at the animal's sensors. Flow visualization indicated that the plume
characteristics appeared identical for the live and dead specimens (see
Results; Figs 3,
4,
5), which suggests that the
breathing current was a mild perturbation to the plume structure. Therefore,
data were collected around the appendages of a dead crab specimen located 0.3m
downstream of the odor source for body orientations between 0° and
90°.

Instantaneous concentration field for (A) an undisturbed plume and (B) a
dead crab specimen oriented at 45°. The filament concentration
(c) is normalized by the source concentration C0,
and the streamwise (x) and cross-stream (y) distances are
normalized by the channel depth H.

Dopamine, prepared in water from the flume at a concentration of 2 mmol
l-1, was used as the chemical tracer in the plume. A
micromanipulator placed the electrode tip at the level of the dorsal carapace
equidistant from the antennules and at the 2nd walking legs on both the right
and left sides at a height of 7.5 mm above the substrate for each body
orientation. After a 1-min interval to assess the baseline activity, 6.0 min
of continuous concentration data were recorded at 5 Hz. The time-average
concentration signal statistically converges within this period for this
highly intermittent plume (Webster and
Weissburg, 2001). The electrode was calibrated immediately prior
to the measurements (using a dilution series encompassing the range of
concentrations seen in the experiment) and showed a linear response to
dopamine concentration (r2>0.95).

Behavior

We characterized blue crab search behavior in chemical plumes to examine
whether animals alter their body orientation in response to drag and odor
presence. Live adult blue crabs, Callinectes sapidus L., were
purchased from a commercial biological supply company and were housed in
saltwater holding tanks adjacent to the flume. Animals were placed in a known
starting position 1.5m downstream of the odor source (9m from the channel
entrance). Attractant odor, created by soaking 7 gl-1 of intact,
fresh shrimp for 30 min in water taken directly from the flume, was released
through the nozzle. Odorless control treatments substituted seawater for
shrimp metabolite solutions.

Trials were performed in near darkness (light intensity ≪1 lux) and
crabs were not responsive to visual disturbances created by human observers.
Red-light-emitting diodes (LEDs), placed dorsally on the left and right sides
of each blue crab before the experiment, allowed us to track the animal in the
flume. A low-light-sensitive CCD camera mounted approximately 2m above the
working section recorded the behavior. Motion analysis software digitally
identified the coordinates of the left and right markers at a rate of 5 Hz to
determine body position and orientation. As in the drag, flow visualization
and electrochemical measurements, orientation angle is defined relative to the
flow. An angle of 0° corresponds to the crab facing directly upstream,
whereas 90° corresponds to the crab facing directly to the side. Not all
animals successfully navigated to the source when releasing the shrimp
metabolite solution. As we cannot discern whether unsuccessful attempts
represent failure to navigate, or a lack of motivation to search, we analyzed
only paths of animals that successfully found the source in the presence of
odor. Details of these methods may be found in previous publications
(Weissburg and Zimmer-Faust,
1993,
1994).

Results

Drag force

Fig. 2 shows the drag
coefficient (CD) data for five crab specimens. The drag
coefficient is maximal at the perpendicular (0°) position and decreases
with increasing angle, showing roughly a 50% decline between 0° and
90°. Variation in CD among the specimens at a given
angle is attributed largely to small variations of body morphology and
appendage position. In these data, Afront is held constant
(at the value for α=0° reported in
Table 1) so the drag force,
which is physically relevant to a foraging animal, is proportional to
CD.

Blake (1985) investigated
the swimming ability of several decapods, including Callinectes
sapidus, by measuring the lift and drag forces on the carapace. Although
he reached similar conclusions regarding the orientation angle that minimizes
CD, these experiments cannot be easily compared with the
current study. In particular, Blake
(1985) performed the
measurements on an isolated carapace, cleaned and smoothed with Plasticine,
and these surgical modifications substantially alter the measured drag
force.

Flow visualization

A flow visualization photograph of the undisturbed plume at a distance of
0.3 meters from the source is shown in Fig.
3A. The plume consists of filaments of high concentration
separated by regions of clear fluid, as reported by Webster and Weissburg
(2001) and Crimaldi et al.
(2002), among others. The
chemical signal arriving at a chemosensor, therefore, is highly fluctuating
and intermittent. The plume spreads gradually and symmetrically (at least in
the time-averaged sense) in the spanwise direction with little meander. The
plume also mixes vertically, although the bed appears to constrain the
downward growth.

Fig. 3B—D are images
of the same plume with the crab at three orientation angles between 0° and
90° (images at increments of 15° for this and another specimen are
available in Percy, 2001). The
purpose of these images is to gain an appreciation of the plume structure at
the chemosensor locations on the claws, legs and antennules. When
perpendicular (0°), the presence of the crab body slightly spreads the
plume and increases the homogeneity of the plume just upstream of the
antennular region, but signals arriving at chemosensors are still visibly
intermittent (Fig. 3B). When
the body is rotated to 45°, the antennular region is located in the wake
of the upstream claw (Fig. 3C).
Turbulence intensity is enhanced in the wake of the claw and the dye plume is
mixed more thoroughly before arriving at the antennules. Thus, the signal
appears more homogeneous at the antennules compared with the undisturbed
plume. At 90°, the plume initially contacts the upstream legs and claw and
the antennules appear to be exposed to little of the plume structure
(Fig. 3D).

Blue crabs have chemosensors on their legs in addition to the sensors on
the antennules. The overhead images show that the flow pattern around the crab
body draws dye under the carapace where it is highly mixed and spread
laterally. These images indicate that the intermittent signal of the
undisturbed plume is clearly not maintained at the legs; they appear to be
completely inundated with a fairly homogeneous dye field. The plume structure
arriving at the legs changes little as orientation angle is increased
(Fig. 3D).

The plume also appears more homogeneous in the wake of the crab than it
does approaching the animal. The plume expands from approximately one-quarter
of the crab body width upstream to nearly the projected width of the crab in
the wake (Fig. 3). The
increased mixing results from the complex flow pattern around the body and
increased local turbulent intensity. The wake narrows as the orientation angle
increases from 0° to 90°, which is consistent with the decrease in
drag coefficient with increasing body angle
(Fig. 3; i.e. a narrower wake
means a lower momentum deficit and, hence, lower drag force).

Flow visualization trials verify that the breathing current affected the
plume minimally, and, hence, flow visualization and measurements around dead
crab specimens are a valid indicator of the true flow properties. Indeed, the
plume characteristics impinging on the dead crab specimen
(Fig. 3C) remain similar for
the live specimen oriented at the same angle
(Fig. 4); in particular, the
plume approaching the animal is filamentous, the wake of the upstream claw
homogenized the plume near the antennules, flow under the carapace spreads the
plume laterally and the legs are inundated with dye, and the wake of the
animal is well mixed and much wider than the upstream plume. Brief excurrent
bursts directed downstream or to the side were observed in the freshwater
trials and, less frequently, in the saltwater trials. These water jets
momentarily add to the turbulence intensity but did not significantly alter
the bulk flow pattern.

Plume structure around the blue crab

Fig. 5 shows the
instantaneous concentration field measured with PLIF in the absence of the
crab and with a dead crab specimen at 45°. The center of the crab is at
x/H=1.5 (i.e. 0.3 m), and the surrounding flat region corresponds to
where the laser sheet is blocked by the crab body. These sample fields again
indicate that the crab body negligibly affects the appearance of the plume
structure approaching from upstream, whereas peak concentrations in the wake
are considerably more dilute due to the presence of the crab body.
Additionally, the peaks are spread out over a broader area in the wake as a
result of the flow disturbance created by the crab body. These observations
support the general impression conveyed in the flow visualization that the
major effect of the crab body is in the downstream wake rather than in the
plume upstream.

Fig. 6A shows the
time-average concentration profiles at a downstream distance of
x/H=2.5 (the center of the crab is at x/H=1.5, thus the
profiles are one channel depth behind the crab). The presence of the animal's
body dilutes the plume significantly; each profile is lower and wider than the
undisturbed profile, which was previously reported in Webster and Weissburg
(2001). The 90°
orientation produced the narrowest profile and highest peak, whereas the
profiles have approximately the same width and concentration peak at
orientations of 0° and 45°. As discussed above, the width of the wake
is consistent with the drag force measurements. Profiles are basically
symmetrical at approximately the center axis at orientations of 0° and
90°, but the 45° orientation shows significant asymmetry resulting
from the skewed geometry of the crab body at this angle. The increased
homogeneity in the wake of the crab also leads to a smaller standard deviation
of the concentration fluctuations (Fig.
6B). The lower S.D. is consistent with the more homogeneous
appearance of the plume in the flow visualization trials (Figs
3,
4). The mean and S.D. values
are of similar magnitude, thus the concentration is still fluctuating greatly
around the mean. The S.D. profiles for 0° and 90° have the largest
S.D. along the centerline. The peak for the 45° orientation is slightly
lower, and the profile shows a second peak at y/H=-0.5, again
suggesting an asymmetric wake for this orientation.

Cross-stream profiles of (A) the filament concentration average
(c̄) and (B) the standard deviation at
x/H=2.5 (see Fig. 5)
for three crab orientations. Concentration is normalized by the source
concentration C0, and the cross-stream distance
(y) is normalized by the channel depth H.

Signal structure at the appendages

Data from the electrochemical sensor quantify the chemical signal structure
at the chemosensors. Fig. 7
shows the concentration of individual odor filaments (conditionally averaged
to include only non-zero readings) and the intermittency factor, defined as
the proportion of time that the concentration is above the detectable limit
(Chatwin and Sullivan, 1989) as
a function of orientation angle. For 0°, the filament concentrations are
relatively high because the plume flow path is unobstructed. As the body is
rotated towards 90°, the antennules and right (downstream) legs receive
signals diluted and mixed by turbulence around the crab's body, and the
concentration diminishes. The left (upstream) leg experiences a slight
increase in the filament concentration as it moves upstream of the body.

Chemical signal characteristics near appendages of dead crab specimens as a
function of body angle. (A) Average filament concentration (c)
normalized by the source concentration C0 and (B)
proportion of samples above the detection threshold (i.e. the intermittency
factor). As shown in Fig. 3,
the left leg moves upstream as the body is rotated from 0° to 90°.

The proportion of time that the signal is above the detection limit is also
affected by body angle. With increased orientation angle, the body becomes a
significant flow obstruction for the downstream legs, resulting in
more-frequent, lower concentration filaments at the antennules and right
(downstream) leg. Signal constancy at the antennules and right (downstream)
leg therefore increases as the body is rotated towards 90° and decreases
at the left leg.

Body orientation behavior

Crabs vary their angular orientation relative to the flow direction
depending on both the flow velocity and odor treatment
(Fig. 8). Crabs orient their
body at an angle nearly parallel (approximately 75°) to the flow except in
low flow with odor present, which results in a smaller mean body orientation
angle (approximately 52°). Odor presence has a significant effect on body
angle for crabs in low, but not high, flow. The distribution of orientation
angles during locomotion also varies with odor presence and flow speed
(Table 2). At high flow, and at
low flow without odor, body orientations are skewed strongly towards high
angles. By contrast, animals tracking odor in low flow often assume low angles
during search. Regardless of flow speed, tracking animals show an increase in
the proportion of low-angle body orientations relative to animals in the
absence of odor. The analysis also reveals that rapid movement speeds of
animals tracking odor plumes in high flows are correlated with high body
angles (r=-0.40, N=941, P≪0.001; cosine
transformation applied to angular data); that is, in these conditions animals
assume high drag postures only when moving slowly. This correlation is not
evident in other groups, possibly because body orientations are strongly
skewed towards high values in the absence of odor, and drag minimization is
not as important for animals navigating through odor plumes in slower
flows.

Distribution of body angles from crab paths in different flow and odor
conditions

Discussion

A combined analysis of hydrodynamic forces, odor signal structure and
behavior indicates that body orientation in blue crabs affects both drag costs
and plume structure. Blue crabs assume specific body angles during movement
that depend on both flow and odor conditions and that have consequences for
the structure of odor signals arriving at their chemosensory appendages as
well as those structures transmitted downstream. The interactions between body
orientation, drag force and plume structure have a variety of implications for
foraging energetics and navigational strategies.

Flow perturbations by the blue crab body

Flow visualization and PLIF images of odor plume structure suggest that
animals exert a negligible effect upstream, but that enhanced mixing in the
turbulent wake significantly altered odor plume structure downstream of the
body for all body orientations. The diminished concentration and increased
homogeneity in the wake of the crab may inhibit the odor-tracking ability of
another downstream predator. This implies a competitive advantage for the
first animal that navigates through the plume, but it seems unlikely that
animals actively manipulate the signal structure downstream.

Although the body does not significantly alter the plume structure
upstream, there is a large influence of the body orientation on the odor
signal structure near the chemosensory appendages. The consequences of this
effect are discussed more fully below.

Behavioral optimization in foraging blue crabs

Drag increases the cost of locomotion, and many animals have evolved body
forms that reduce drag and, therefore, the energy required for propulsion
(Vogel, 1994). Decreased drag
also promotes stability against overturning, which offers significant
advantages for substrate-bound aquatic creatures such as crabs
(Martinez et al., 1998;
Martinez, 2001). Given the
nearly twofold variation in CD, Callinectes can
reduce its cost of locomotion substantially by assuming body angles near
90°. Crabs in high and low flow in the absence of odor oriented at angles
very near the drag-minimizing posture; the corresponding
CD at 75° is only 10% higher than the smallest
measured value.

Although crabs assume body angles with relatively small drag, they rarely
adopt a drag-minimizing posture (i.e. 90°) and, in the presence of odor,
more frequently assume orientations with higher drag. The mean angle of
animals navigating to odor plumes in low flow was 52°, which is
approximately midway between drag-minimizing and -maximizing orientations. By
orienting at this angle, crabs increased CD by nearly 40%
relative to the other treatment. A low mean angle was observed in slow flow
only when odor was present, suggesting that changes in body orientation were
not solely a response to relaxed energetic penalties in slower flows. Rather,
there appears to be a tradeoff between drag minimization and tracking ability
that encourages animals navigating in odor plumes to assume orientations that
do not minimize drag. This tradeoff was evident to a smaller degree in high
flows, where animals tracking odors orient at low angles during slow movement
when drag costs are potentially smaller.

The propensity of foraging crabs to adopt a higher drag orientation appears
to be related to its ability to acquire useful chemosensory cues. Analysis of
chemical signals impinging on chemosensory appendages reveals a significant
influence of body orientation and illustrates how signals more conducive to
odor tracking occur at low body angles. Blue crabs, and perhaps other
crustaceans, rely on an up-current response triggered by detecting odor
filaments (Weissburg and Zimmer-Faust,
1993; McLeese,
1973). Orienting at low angles brings chemosensors on the antennae
and antennules into contact with less-dilute odor signals. As rapid dilution
in turbulent odor plumes may quickly render even highly concentrated stimuli
below typical detection thresholds for crustacean chemosensors, orientation at
low body angles enhances the perception of relevant odors. Plume tracking also
utilizes the asymmetry of odor arrival at bilaterally paired sensory
appendages such as legs and antennules
(Reeder and Ache, 1980;
Devine and Atema, 1982;
Zimmer-Faust et al., 1995).
Animals react to signal contrast between sensors separated in the cross-stream
direction by steering towards the more intensely stimulated side, which keeps
them close to the main axis of the plume. Larger sensor spans in the
transverse direction improve the signal contrast
(Webster et al., 2001).
Appendages span a larger cross-stream distance at low body angles, whereas at
90° there is minimal transverse separation because paired appendages are
aligned with the plume axis. Additionally, chemosensors on the legs experience
differences in frequency and intensity of stimulation, as one member of the
pair is located in the wake of the body. Thus, the asymmetric perturbation of
the signal at the leg chemosensors further compromises the animal's ability to
determine the lateral position relative to the plume centerline.

Although the precise form of the tradeoff behavior is not known, the data
indicate that crabs assume a higher drag orientation when searching for an
odor source via an odorgated rheotaxis strategy with bilateral
comparison. Thus, crabs appear willing to accept a higher drag force, and
higher cost of locomotion, in order to acquire useful chemosensory information
under some circumstances. The tradeoff has limits, however. For instance,
crabs do not orient at 0°, which provides the strongest signal at the
antennules and the best contrast between the leg chemosensors but has the
disadvantage of dramatically increasing the drag force. Furthermore,
minimizing the drag coefficient is particularly important in high flow because
the drag force increases in proportion to the square of velocity (equation 2).
Thus, crabs appear unwilling to orient with a high drag coefficient in higher
speed flows even in the presence of odor.

Constraints on information gathering

Blue crabs increase their cost of locomotion in order to successfully track
odor sources, thus increasing the cost of chemical information gathered during
foraging. Economic models of consumer behavior do not generally incorporate
costs associated with constraints on sensory systems. However, evidence is
accumulating that perceptual mechanisms impose costs on foraging energetics
and may have a significant impact on behavior (e.g.
Barclay and Brigham, 1994;
Spaethe et al., 2001). Animals
locating or discriminating objects in flow may respond by either tolerating
these costs or reducing them at the expense of sensory information. Blue crabs
display clear evidence of these tradeoffs, orienting themselves to increase
the availability of chemical signals in slow flows but minimizing the cost of
drag in high flows. Such tradeoffs may be common in other organisms using
olfactory cues in flow. For instance, moths change their body angle when
flying in different conditions, becoming more parallel to both the ground and
the wind direction as wind velocity increases
(Wilmott and Ellington, 1997;
Zanen and Cardé, 1999).
This behavior minimizes the frontal area to reduce the drag of moths in
flight, but places their chemosensors more directly in line with the body.
Thus, upstream propagation of fluid disturbances (e.g. bow wakes) may affect
chemical signal structure impinging on sense organs close to the body. Whether
postural adjustments reducing drag in response to high wind velocity also
degrade or change chemical signals impinging on olfactory receptors remains
unknown. Spiny lobsters (Panulirus argus) reduce the spread of their
antennae during locomotion in proportion to increasing flow velocity.
Interestingly, they never adopt a spacing that minimizes drag, perhaps because
greatly reducing their antennae spread interferes with their ability to
acquire sensory input (Bill and Herrnkind,
1976). In general, tradeoffs between costs associated with sensory
perception vs other behavioral requirements have not been examined in
detail. As suggested here, these tradeoffs are liable to be critically
important for cost—benefit models of food finding or other resource
acquisition behaviors that utilize chemically mediated guidance.

Flow velocities in habitats occupied by benthic animals change both
spatially, as a result of variations in the depth or width of inlets and
channels, and temporally during tidal cycles. Crabs adjust their foraging
strategy in response to the perceived energetic costs and potential benefits
of enhanced foraging efficiency for given conditions. This behavioral
flexibility indicates that crabs integrate these potential costs and benefits
so that they only assume a high drag posture when the costs are low and odor
stimuli indicative of a potential energetic reward are present. Foraging
models sometimes incorporate tradeoffs between foraging and other activities,
such as predator avoidance or reproduction (e.g.
Lima and Dill, 1990;
Mangel and Ludwig, 1992). The
underlying constraint is that time cannot be allocated simultaneously to two
activities, so that the energetic cost of lost foraging opportunity is offset
by the benefits of increasing time spent performing another task. Nearly all
models of foraging tradeoffs are similarly formulated in terms of time
allocation. However, this is not an appropriate model for tradeoffs involving
conflicting constraints that balance expected energetic penalties during
locomotion with energetic gains associated with more-effective odor tracking,
because these two activities occur simultaneously. Animals may choose flow
habitats based on these cost—benefit functions, and the ability of
animals to forage effectively in flow has substantial impacts on community
properties (Leonard et al.,
1998). Different modeling approaches, as well as further insights
on chemical signal transmission and reception, will be necessary to assess
tradeoffs between locomotion and chemoperception and how this may translate
into patterns of habitat choice and predatory intensity.

Navigational strategies in turbulent plumes

Terrestrial and aquatic arthropods use rapidly acquired cues in highly
intermittent turbulent odor plumes to navigate towards an odor source
(Weissburg, 2000;
Vickers, 2000). This has led
to a widely shared opinion that turbulence is the relevant flow property for
explaining tracking success, an idea that has been verified using behavioral
experiments decoupling turbulence intensity from bulk flow velocity
(Weissburg and Zimmer-Faust,
1993). Thus, it is somewhat ironic to discover that flow speed may
also impact tracking success by causing behavioral changes that alter signal
acquisition ability. Future efforts to understand olfactory processes in flow
need to carefully distinguish among physical effects due to changes in signal
structure and flow-induced modifications in behavioral and sensory processes
that modulate the ability of animals to acquire information from those
chemical signals.

ACKNOWLEDGEMENTS

The authors would like to thank Troy Keller, Sharon Palmer, Prasad Dasi,
Matt Ferner and Mariann Vandromme for their assistance in the lab. ONR/DARPA
provided financial support for this project (N00014-98-1-0776).

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